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First published online March 16, 2007
Journal of Experimental Biology 210, 1139-1147 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02741
Disruptive coloration in cuttlefish: a visual perception mechanism that regulates ontogenetic adjustment of skin patterning
1 Marine Resources Center, Marine Biological Laboratory, 7 MBL Street, Woods
Hole, MA 02543, USA
2 Department of Cognitive Sciences and Institute for Mathematical Behavioral
Sciences, University of California at Irvine, USA
3 Department of Life Science, National Tsing Hua University, Hsinchu, 30013,
Taiwan
* Author for correspondence (e-mail: abarbosa{at}mbl.edu)
Accepted 29 January 2007
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Summary |
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For each of seven size classes of cuttlefish, we created black and white checkerboards whose check sizes corresponded to 4, 12, 40, 120, 400 and 1200% of the area of the cuttlefish's White square, which is a neurophysiologically controlled component of the skin. Disruptive body patterns were evoked when, regardless of animal size, the check size measured either 40 or 120% of the area of the cuttlefish's White square, thus demonstrating a remarkable ontogenetic conformity to a single visual sampling rule.
Cuttlefish have no known visual feedback loop with which to adjust their skin patterns. Since the area of a cuttlefish's White square skin component is a function of body size, our results indicate that cuttlefish are solving a visual scaling problem of camouflage presumably without visual confirmation of the size of their own skin component.
Key words: camouflage, Sepia officinalis, visual sensori-motor system, crypsis, chromatophore, cephalopod
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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;
Edmunds, 1974). Crypsis
through background matching requires that colors, sizes and shapes of the body
pattern components should resemble those of the visual background
(Cott, 1940;
Edmunds, 1974;
Endler, 1978;
Merilaita, 1998). In
disruptive coloration, camouflage is achieved when the animal's outline is
broken up into patches of different size, shape, contrast, color, etc., such
that the observer's attention is drawn away from the animal's shape, thus
decreasing the animal's chance of being detected
(Cott, 1940;
Edmunds, 1974;
Stevens and Cuthill, 2006).
Furthermore, according to Schaefer and Stobbe
(Schaefer and Stobbe, 2006),
disruptive coloration on an animal's edge is an effective camouflage method
independently of the background. Recent studies have tested experimentally the
principles of both background matching and disruptive coloration and this is
an active area of discussion (see
Merilaita et al., 2001;
Cuthill et al., 2005;
Cuthill et al., 2006;
Merilaita and Lind, 2005;
Schaefer and Stobbe, 2006;
Stevens et al., 2006).
Cephalopods (squid, octopus and cuttlefish, Phylum Mollusca, Order
Cephalopoda) are unique in the animal kingdom because of their exceptional
neurophysiologically controlled skin that allows for rapid changeable
coloration, enabling them to achieve dynamic crypsis in a wide range of
habitats (cf. Holmes, 1940;
Packard and Sanders, 1971;
Packard and Hochberg, 1977;
Hanlon and Messenger, 1988;
Hanlon and Messenger, 1996).
Cephalopod skin can vary in pattern, color, brightness/contrast and texture,
allowing the animals to produce an overall repertoire of 20–50 body
patterns (defined as the total appearance of the animal) that serve a variety
of behavioral functions. This changeable repertoire of adaptive coloration is
achieved by a system of dermal pigmented organs, or chromatophores,
complemented by structural reflectors called iridophores and leucophores
(Hanlon, 1982;
Cloney and Brocco, 1983;
Messenger, 2001).
The cuttlefish's many body patterns used for camouflage can be reduced to
three general categories: uniform/stipple, mottle and disruptive
(Hanlon and Messenger, 1988).
Uniform/stipple body patterns are used to match generally uniform backgrounds.
On non-uniform backgrounds, cuttlefish show mottle or disruptive body patterns
for crypsis. Mottle patterns consist of alternating, irregularly shaped,
semi-round small dark and light patches in the skin that correspond roughly to
the size of dark and light objects in the visual background. Emulating the
small dark and light objects of the background in its mantle helps cuttlefish
resemble the non-uniformity of many natural backgrounds. Disruptive body
patterns are irregular patches of different shape orientation (transverse and
longitudinal bars, squares and other shapes), contrast and color that serve to
distract the observer's attention from the outline of the animal. In the
common European cuttlefish Sepia officinalis (Linnaeus 1758),
disruptive patterning is most commonly characterized by variable expression of
five light and six dark chromatic components
(Fig. 1). Each component is an
independent neurophysiological entity that can be shown singly or in
combination with other components in differing strengths of expression
(Hanlon and Messenger, 1988).
Among these 11 disruptive components, the White square of a cuttlefish (2 in
Fig. 1) is bold and often
white. Crypsis is achieved, at least partly, because the White square is
expressed when other light objects of similar size are in the visual
background, thus rendering the animal's White square as a random sample of
other light objects in the background.
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).
It illustrates how cuttlefish of different sizes can adopt different
camouflage tactics on the same visual background. The composite photograph
shows a hatchling cuttlefish (left), an early juvenile (right), and a late
juvenile (center) on the same background of coarse gravel. The smallest animal
is showing a strong disruptive pattern, the early juvenile a weak disruptive,
and the largest animal a light mottle, even though the pebble size is the
same. The dimensions of some of the light and dark components of the hatchling
are close to those of the gravel, so that the disruptive pattern is
appropriate; the dimensions of the late juvenile are already such that
disruptive components, if expressed, would exceed the gravel sizes in the
background. This illustrates that for S. officinalis, an important
feature of concealment on a given background is related to the size of the
animal, as they must be able to estimate the substrate particle size so that
they show the appropriate body pattern
(Hanlon and Messenger,
1988).
|
;
Hanlon and Messenger, 1996;
Marshall and Messenger, 1996;
Chiao and Hanlon, 2001a;
Chiao and Hanlon, 2001b;
Chiao et al., 2005;
Mäthger et al., 2006).
Chiao and Hanlon developed a noninvasive, quantifiable methodology using
computer-generated images to study body patterning in Sepia pharaonis
(Chiao and Hanlon, 2001a;
Chiao and Hanlon, 2001b). The
observation that visual stimuli lead to changes in body patterns of the skin
(motor output) allows detailed analysis of visual perception in cuttlefish.
Based on Holmes (Holmes, 1940)
and Hanlon and Messenger (Hanlon and
Messenger, 1988), Chiao and Hanlon showed that the main visual
features that cuttlefish key on for producing disruptive coloration are area,
contrast, and density of white elements on a dark background
(Chiao and Hanlon, 2001a;
Chiao and Hanlon, 2001b). The
same methodology was adopted in subsequent studies in S. officinalis
to show that disruptive body patterning requires visual information on edges
and contrast of objects in natural substrates
(Chiao et al., 2005) and to
demonstrate behaviorally that they are colorblind
(Mäthger et al., 2006)
(see also Marshall and Messenger,
1996).
Previously it was found that juvenile S. pharaonis consistently
responded to white and black checks by showing disruptive coloration
(Chiao and Hanlon, 2001a). We
have shown that this is also true in S. officinalis
(Mäthger et al., 2006),
but to date ontogenetic variations in this behavior have not been tested.
Although hatchling and juvenile S. officinalis have been reported to
show ontogenetic variations in response to natural substrates
(Hanlon and Messenger, 1988;
Poirier et al., 2005), this is the first study investigating the disruptive
behavior across all developmental stages (from hatchling to adult). Chiao and
Hanlon's studies on artificial backgrounds
(Chiao and Hanlon, 2001a;
Chiao and Hanlon, 2001b) used
only the analysis of the White square component as a measure of disruptive
coloration. In the present study, the grading analysis was expanded to 11 body
pattern components, and an extensive set of experiments was conducted to study
the visual perception of a variety of sizes of light objects (white checks) in
the visual background. The present paper demonstrates experimentally that
cuttlefish of widely different sizes apparently use a simple visual sampling
rule to account for scaling issues in disruptive coloration.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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;
Hanley et al., 1998)]. Seven
experiments were conducted from June 2003 to August 2005. All cuttlefish were
housed separately for the duration of the experiments. The mantle lengths (ML)
and White square (WS) areas of the animals were derived from digital images of
the cuttlefish on a known size of white and black checkerboard using NIH Image
1.62 (US National Institute of Health;
http://rsb.info.nih.gov/nih-image/).
For each experiment, six checkerboards with check areas of 4%, 12%, 40%, 120%,
400% and 1200% of the cuttlefish's mean WS area were computer generated,
printed and laminated to be waterproof. Check areas were chosen based on a
logarithmic scale. For example, for cuttlefish of size class 2, the check
areas were 0.01, 0.03, 0.1, 0.3, 1 and 3 cm2; the log of each area
corresponds to an increment of 0.5. Each experiment corresponds to a
cuttlefish size class. Table 1
provides all measurements.
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To determine the checkerboards' contrast, relative reflectance spectra of
check colors (i.e. pure white and pure black, equivalent to 0 and 255
intensity levels, where 0 is black and 255 is white) were measured using a
fiber optic spectrometer (USB2000, Ocean Optics, Florida USA). A detailed
description of the method used to calculate the apparent contrast as perceived
by the cuttlefish eye is published elsewhere
(Mäthger et al., 2006).
Checkerboards' contrast ranged between 84 and 95%.
For experimentation, cuttlefish were placed inside either a rectangular
divider or a circular arena with the following dimensions (cm) to accommodate
growing cuttlefish: Experiment 1: 9.2x4 diameterxheight;
Experiment 2: 28x20x11 lengthxwidthxheight; Experiment
3: 28x20x11 lengthxwidthxheight; Experiment 4:
24.5x10 diameterx height; Experiment 5: 24.5x14.5
diameterxheight; Experiment 6: 38x26x21
lengthxwidthxheight; Experiment 7: 28x33.5x21
lengthxwidthxheight. The inside of the divider/arena was lined
with black felt. This set-up was placed inside a running seawater tank
surrounded by black felt and black plastic sheeting. Animals were allowed to
move freely inside the arena and their body pattern was recorded using a
digital camera, mounted above the tank. The camera was set to record 2 s every
minute, and connected to an external monitor to allow remote viewing to reduce
disturbance to the animals and experimenter bias
(Boal, 1996). Recording began
only when the animals were acclimated. Acclimation (i.e. cessation of
excessive swimming and hovering movements and expression of stable body
pattern) period was at least 5 min.
Image analysis: grading body pattern responses
Each trial lasted 30 min, yielding 60 s of recorded footage. For analysis,
a frame was taken every 6 s from the recorded video footage (10 images per
trial), yielding a total of 2720 images for the entire experiment. Eleven skin
components of disruptive coloration were graded for each image (see
Fig. 1). Each component was
graded from 0 to 3 (0, not expressed; 1, weakly expressed; 2, moderately
expressed; and 3, strongly expressed) (see
Fig. 3 for an example of
grading). According to this grading scheme, an animal could be given a total
grade ranging from 0 (no expression of any disruptive component) to 33 (all
disruptive components strongly expressed, i.e. 3x11=33). This method has
been used previously (Mäthger et al.,
2006). We averaged grades of all 10 images obtained for each
animal on each substrate.
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Statistical analysis
We found disruptive scores to be normally distributed, and therefore
conducted a mixed model ANOVA (Zar,
1999), including a within-subjects factor of check area and a
between-subjects factor of cuttlefish size class. We tested if different check
areas elicited different disruptive responses, if the different size classes
responded differently to the experimental substrates, and finally if there was
an interaction between check area and size class. Such interaction would
indicate that animals of different absolute size responded in significantly
different ways when exposed to substrates scaled equivalently to their White
square area. Analyses first included all six substrates and were subsequently
restricted to the 40% and 120% check areas. Statistical analyses were
performed using SPSS 14 (SPSS Inc.).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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Fig. 5 shows the average disruptive coloration scores of the seven size classes for all six check areas. In all size classes, the highest disruptive scores were recorded on checkerboards with check sizes of either 40% or 120% of the area of the animal's White square (values within gray rectangle). For each size class, there was a tendency for the disruptive scores to progressively increase and then decrease with the increasing ratio of check area to White square area.
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A mixed model ANOVA disclosed significant main effects of check area (P<0.001) and size class (P<0.001). Therefore, it is apparent from this result that different check areas evoked different responses by the animals and that the strength of the disruptive response differed among size classes. However, a significant interaction between check area and cuttlefish size class was also detected (P<0.001), which indicates that individuals of the different size classes responded in significantly different ways when exposed to the various treatments (see below).
Ontogenetic variations in disruptive responses to check areas of 40% and 120% of the mean area of the cuttlefish's White square
A glance at Fig. 5 shows
that the check area–size class interaction is focused primarily on the
40% and 120% check areas of the mean area of White square. Here we see one of
the most notable differences between size classes. Larger animals (size
classes 6 and 7) gave stronger disruptive responses on the 40% check area than
on the 120% check area, whereas this pattern was reversed for size classes
1–5. To examine this interaction more carefully, we conducted another
mixed model ANOVA including only the 40% and 120% check areas as
within-subjects factor. As anticipated, the check area–size class
interaction was highly significant (P<0.001).
Fig. 6 shows the strength of
the disruptive response on the 40% and 120% check areas for all size classes.
The plot reveals quite strikingly that the interaction is due exclusively to a
difference in behavior between size classes 6 and 7 versus size
classes 1–5. Indeed, size classes 1–5 revealed no internal
interactions. The curves for the 40% and 120% check areas are nearly parallel
across size classes 1–5, and a mixed model ANOVA restricted to size
classes 1–5 and check areas 40% and 120% of the mean area of White
square yielded no significant check area by size class interaction
(P=0.730).
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Qualitative and quantitative differences in the composition of disruptive components
To analyze differences among the expression of the eleven disruptive skin
components, we looked at the relative expression of each component on the 40%
and 120% check areas (Fig. 7).
We grouped the seven size classes in three major groups: small (size classes 1
and 2), medium (size classes 3, 4 and 5) and large (size classes 6 and 7). For
each category, we took the mean score of each component and divided it by the
sum of all component scores, yielding a final normalized value, with the sum
of all normalized values adding to 1. This enabled us to evaluate whether a
component was commonly expressed or not, independently of the strength of its
expression. The relative level of disruptive components expression differed
among groups. The normalized data revealed that the small and medium groups
are quite similar in the disruptive components shown. However, the large group
produced normalized scores that are significantly lower than those of the
other two groups on components White posterior triangle (WPT) and Median
mantle stripes (MMS). This same trend holds true if we look separately at the
disruptive scores at the 40% or 120% check areas (data not shown).
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These results suggest that, although cuttlefish in all size classes can show complex disruptive body patterns, different tactics seem to be adopted ontogenetically to achieve disruption. This can be seen both in the disruptive components expressed and how strongly they are expressed, as well in the combinations of those disruptive components.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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Effect of check sizes on body patterning
For each size class of cuttlefish, differently sized checkerboards of high
contrast and sharp edges evoked all three camouflaged body pattern types:
uniform, mottle and disruptive. The focus of this paper is on disruptive
coloration, and the main finding is that checks of 40% and 120% of the mean
area of the White square evoked disruptive patterns with noteworthy
consistency throughout all sizes of cuttlefish. When checks were much larger
than the mean area of the White square, i.e. 400% and 1200%, uniform and some
disruptive patterns were evoked. Currently, we do not have a good explanation
for the responses to large checkerboards. Responses to larger check areas
suggest that the sampled visual field by each cuttlefish eye may be different
enough to influence the pattern type. For example, depending on the position
on the substrate, a cuttlefish may occupy part of a large white check and may
therefore only see a small portion of it, and as a result show disruptive
patterning. Conversely, if a fully visible large check predominates the
immediate visual field of a cuttlefish, then a uniform pattern might be
expected. When checks were small (i.e. 4% and 12% area of the White square)
mottle was a common but not exclusive response
(Fig. 4). This response was not
as surprising, since previously we have noted that small checkerboards of high
contrast and sharp edges tend to evoke mottle patterns
(Barbosa et al., 2004).
However, a good deal of work remains to determine experimentally the visual
background features that evoke mottle.
Ontogenetics changes in disruptive patterning
Animals undergo a number of changes during ontogeny, and a particular
function (e.g. behavioral, physiological, morphological, etc.) can shift as
body size changes (Koehl,
2000). In most animals, ontogenetic color changes are
nonreversible, and they are associated with normal progressive development of
an animal (e.g. Booth, 1990).
Such color changes occur in marine and terrestrial invertebrates, fish,
amphibians, reptiles, birds and mammals, and are often associated with changes
in size, vulnerability, reproductive status, habitat and metabolism. In
cuttlefish, color changes are not fixed, and animals can change rapidly from
one pattern to another. The notion of ontogenetic changes in body patterning
of Sepia officinalis is not novel. Changes in camouflage tactics
between hatchlings and adults result from a shift in emphasis from crypsis to
communication (especially sexual signaling), with adults exhibiting the zebra
body pattern (Hanlon and Messenger,
1988; Hanlon and Messenger,
1996). In addition, the density of chromatophores has been shown
to decrease with age (Hanlon and
Messenger, 1988; Hanlon and
Messenger, 1996). Even though S. officinalis may be able
to change rapidly between particular camouflaged body patterns, the
combination of disruptive components shown may not be as flexible, with adult
animals showing different combinations of disruptive components compared to
young animals (Table 2).
Furthermore, some disruptive components appear to be almost completely dropped
with cuttlefish age (Fig. 7).
Morphologically, the higher density of chromatophores in hatchlings compared
to adults (Hanlon and Messenger,
1988) may explain why smaller animals were more disruptive than
larger animals. A higher density of chromatophores may imply that small
cuttlefish are capable of expressing a given component more strongly and with
greater fine tuning.
From our study, we can conclude that disruptive patterning in S. officinalis appears to undergo three main changes during ontogeny: (1) the degree of disruptive coloration decreases with age (Figs 5 and 6), (2) the types of components change, with some components shown more frequently in one age group, and less so in other age groups (Fig. 7), and (3) the combinations of disruptive components expressed also change with age of animal (Table 2).
Visual perception and background features
Work on young S. officinalis showed that when animals are placed
on the same particle size, body patterning changes dramatically during
ontogeny [Fig. 2 (see also
Hanlon and Messenger, 1988)].
In the present study, we extended this observation to a wider range of animal
sizes. For example, it is interesting to look at the body patterning response
of cuttlefish of different sizes placed on a similar checkerboard size. On a
0.84 cm2 checkerboard (1200% check area), hatchlings (size class 1)
responded with a uniform body pattern, whereas adults (size class 6) placed on
a 0.88 cm2 (4% check area) responded with a mottle body pattern
(Fig. 4). It is clear that for
cuttlefish of different sizes, body patterns chosen on a checkerboard with a
very similar area are related to the animal's size.
Our results indirectly address how cuttlefish scale their body patterns:
they apparently cue visually on light objects in the visual background. Since
the cuttlefish mantle has a convex shape, it appears likely that a cuttlefish
cannot see its White square component. Indeed, blocking their posterior field
of view by placing a plastic ruff around the head does not seem to prevent
cuttlefish from showing an appropriate camouflage body pattern [see fig. 34 in
Messenger (Messenger, 2001)],
suggesting that cuttlefish do not require visual confirmation of their body
pattern when deciding what camouflage pattern to show. It therefore seems
likely that the animals do not visually inspect their skin components; i.e.
their visual sensori-motor system does not rely on a feedback response.
A few other animals are also faced with the problem of what body patterns
to show on a given substrate. For example, the skin of the tropical flatfish
Bothus ocellatus is believed to be under neural control, changing
within 2–8 s, but mechanisms of visual control of patterning remain
undetermined (Ramachandran et al.,
1996; Kelman et al.,
2006). In cephalopod studies, it is clear that cuttlefish cannot
adjust the size of each physiological skin component for disruptive
coloration, although they can express each component in different intensities.
For example, the size of the White square is fixed relative to the animal's
mantle length. It continues to intrigue us that the same visual input can lead
to different motor output in animals of different sizes. Unfortunately, visual
processing in cephalopods is poorly studied
(Messenger, 1991), thus it is
impossible to provide any useful speculation about neural mechanisms of
perception ontogeny. The cuttlefish's responses on small check areas indicate
that cuttlefish of all sizes possess high visual acuity. As stated by Groeger
et al. in their study on the ontogenetic changes in visual acuity of S.
officinalis (Groeger et al.,
2005), at very early stages of development cuttlefish already have
acute vision, although this acuity improves in larger animals.
This study is limited insofar as the experiments dealt with only one detail
of the background checks: size (measured as area). In addition, it is accepted
that contrast between light and dark objects in the background, as well as
object edges, are essential visual cues to turn on disruptive coloration
(Chiao and Hanlon, 2001a;
Chiao et al., 2005;
Mäthger et al., 2006).
According to Chiao and Hanlon (Chiao and
Hanlon, 2001a) and Mäthger et al.
(Mäthger et al., 2006), a
contrast sensitivity of ca. 15–20% represents the minimum contrast level
necessary to trigger the full expression of one disruptive component. In the
present paper, contrast (>84%) and edge information were held constant;
therefore, from this study we cannot make any inferences about their weight in
determining disruptive coloration in cuttlefish, nor their role in the
ontogeny of body patterning. One limitation of this work is that we used six
specific check areas: 4, 12, 40, 120, 400 and 1200% of cuttlefish White square
area. Previous work (Mäthger et al.,
2006) used 100% as the standard size that evoked disruptive
coloration in S. officinalis, thus we are confident that 40, 100 and
120% will evoke disruptive coloration in S. officinalis. However, we
cannot draw accurate conclusions about cuttlefish pattern responses below 40%
or higher than 120%. Although the purpose of this study was not to establish
all the visual features that turn on disruptive coloration, we can infer from
our results that light objects in a highly contrasting visual environment with
well-defined edges are an important visual cue necessary to evoke disruptive
coloration in any sized cuttlefish.
Consistent with the initial research on this topic on S. pharaonis
(Chiao and Hanlon, 2001a),
S. officinalis responded with different body patterns to
checkerboards of different sizes. However, S. officinalis showed
disruptive patterning on a broader range of check areas than S.
pharaonis. Both species have a wide geographical distribution. Sepia
pharaonis is found in tropical waters, whereas S. officinalis
can be found in a variety of temperate environments. Little is known about the
ethology of either species under natural conditions, yet from our results, we
speculate that there may be a larger variety of light objects in the visual
backgrounds throughout the range of S. officinalis. However, no one
has characterized visual backgrounds in any of these natural habitats with
these sorts of features under consideration.
Future studies that explore the effective light areas of the background that elicit disruptive patterns may help us understand differences in visual perception and pattern scaling between large and small animals. We used a greatly simplified visual background stimulus – a high-contrast checkerboard – to decipher this `visual sampling rule.' We hope this information can guide us and others to understand cuttlefish responses to natural substrates.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of abbreviationsReferences |
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